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Fukuyama, Yuto; Omae, Kimiho; Yoshida, Takashi; Sako, Author(S) Yoshihiko

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Fukuyama, Yuto; Omae, Kimiho; Yoshida, Takashi; Sako, Author(S) Yoshihiko Transcriptome analysis of a thermophilic and hydrogenogenic Title carboxydotroph Carboxydothermus pertinax Fukuyama, Yuto; Omae, Kimiho; Yoshida, Takashi; Sako, Author(s) Yoshihiko Citation Extremophiles (2019), 23(4): 389-398 Issue Date 2019-07 URL http://hdl.handle.net/2433/243263 © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which Right permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Type Journal Article Textversion publisher Kyoto University Extremophiles (2019) 23:389–398 https://doi.org/10.1007/s00792-019-01091-x ORIGINAL PAPER Transcriptome analysis of a thermophilic and hydrogenogenic carboxydotroph Carboxydothermus pertinax Yuto Fukuyama1 · Kimiho Omae1 · Takashi Yoshida1 · Yoshihiko Sako1 Received: 9 January 2019 / Accepted: 21 March 2019 / Published online: 3 April 2019 © The Author(s) 2019 Abstract A thermophilic and hydrogenogenic carboxydotroph, Carboxydothermus pertinax, performs hydrogenogenic CO metabolism in which CODH-II couples with distally encoded ECH. To enhance our knowledge of its hydrogenogenic CO metabolism, we performed whole transcriptome analysis of C. pertinax grown under 100% CO or 100% N2 using RNA sequencing. Of the 2577 genes, 36 and 64 genes were diferentially expressed genes (DEGs) with false discovery rate adjusted P value < 0.05 when grown under 100% CO or 100% N2, respectively. Most of the DEGs were components of 23 gene clusters, suggesting switch between metabolisms via intensive expression changes in a relatively low number of gene clusters. Of the 9 signif- cantly expressed gene clusters under 100% CO, CODH-II and ECH gene clusters were found. Only the ECH gene cluster was regulated by the CO-responsive transcriptional factor CooA, suggesting that others were separately regulated in the same transcriptional cascade as the ECH gene cluster. Of the 14 signifcantly expressed gene clusters under 100% N2, ferrous iron transport gene cluster involved in anaerobic respiration and prophage region were found. Considering that the expression of the temperate phage was strictly repressed under 100% CO, hydrogenogenic CO metabolism might be stable for C. pertinax. Keywords Hydrogenogenic carboxydotroph · Carbon monoxide dehydrogenase · RNA sequencing · Carboxydothermus pertinax Abbreviations 1992). Owing to the low redox potential (− 520 mV) of CO CODH Carbon monoxide dehydrogenase (Grahame and DeMoll 1995), anaerobic carboxydotrophs ECH Energy-converting hydrogenase can couple CO oxidation to various reduction reactions such DEG Diferential expression gene as sulfate to sulfde (sulfate-reducers), water to H 2 (hydrog- 3+ 2+ LTTR​ LysR-type transcriptional regulator enogens), Fe to Fe (Fe[III]-reducers), and CO2 to acetate (acetogens) or methane (methanogens) (Oelgeschläger and Rother 2008; Sokolova et al. 2009). Many anaerobic and Introduction thermophilic carboxydotrophs have been isolated (Sokolova et al. 2009) from hydrothermal environments where CO is Carbon monoxide (CO) is toxic for many organisms. How- supplied by volcanic gas, photochemical and thermochemi- ever, some prokaryotes, called CO-utilizing microbes (car- cal decomposition of organic matter, and as a by-product boxydotrophs), can use CO as the source of energy and of certain thermophiles (King and Weber 2007; Techtmann carbon for their growth (CO metabolism) (Mörsdorf et al. et al. 2009). Among them, 25 strains representing 13 gen- era (21 species) have been reported as hydrogenogenic car- boxydotrophs (Sokolova and Lebedinsky 2013). Recently, Communicated by A. Driessen. in addition to these 25 strains, three thermophilic and Electronic supplementary material The online version of this hydrogenogenic carboxydotrophs, namely Thermococcus article (https ://doi.org/10.1007/s0079 2-019-01091 -x) contains barophilus (Kozhevnikova et al. 2016), Thermoanaerobac- supplementary material, which is available to authorized users. ter kivui (Weghof and Müller 2016), and Parageobacillus thermoglucosidasius * Yoshihiko Sako (Mohr et al. 2018), have been reported. [email protected] Although a number of strains of Moorella thermoacetica have been isolated, only one strain (M. thermoacetica strain 1 Division of Applied Biosciences, Graduate School AMP) exhibits hydrogenogenic carboxydotrophy, whereas of Agriculture, Kyoto University, Kyoto 606-8502, Japan Vol.:(0123456789)1 3 390 Extremophiles (2019) 23:389–398 the other strains are acetogenic carboxydotrophs (Jiang et al. contact with RNA polymerase (Leduc et al. 2001). In the 2009). Because of their ability to use potentially toxic CO R. rubrum genome, CODH gene cluster and ECH gene and produce H2 as the source of energy for other microbes, cluster are closely arranged and the CooA-binding site is hydrogenogenic carboxydotrophs are assumed to be impor- found upstream of both cooF in the CODH gene cluster and tant ‘CO scavengers’ and primary producers in the envi- cooM in the ECH gene cluster (Fox et al. 1996; Rajeev et al. ronment (Sokolova and Lebedinsky 2013; Techtmann et al. 2012). The previous study shows that CooA homologs are 2009; Yoneda et al. 2013, 2015). divided into two phylogenetically distinct groups (CooA-1 In anaerobic carboxydotrophs, CODH, with Ni in its and CooA-2). CooA-1 is found in the majority of CooA pos- active center, catalyzes the oxidoreductive interconver- sessing carboxydotrophs, whereas CooA-2 is found in some sion between CO and CO 2 (Ragsdale 2004). The function carboxydotrophs that possess multiple CODH gene clusters of CODH has been principally predicted by the genomic in their genomes (Techtmann et al. 2011). Furthermore, CO- context of each CODH gene (cooS; Techtmann et al. 2012). binding assay of two CooA groups shows that both CooA-1 A model of hydrogenogenic carboxydotrophs, Carboxydo- and CooA-2 are in their active forms in high CO concentra- thermus hydrogenoformans, possesses fve genes (cooS-I to tion, whereas only CooA-2 is in active form even in low CO -V) which code for the catalytic subunits of CODHs (CODH- concentration (Techtmann et al. 2011). This diference in CO I–V) on its genome (Wu et al. 2005). Based on the genomic activation in the two CooA groups enables the bacterium to context of the gene clusters including each cooS and/or regulate multiple CODH gene clusters across wide range empirical evidence, their functions are predicted as follows: of CO concentrations (Techtmann et al. 2011). In addition CODH-I, energy conversion conjugated with ECH; CODH- to CooA, recent studies have reported other anaerobic CO- II, NAD(P)H generation; CODH-III, carbon fxation in the responsive transcriptional factors RcoM and CO-responsive Wood–Ljungdahl pathway conjugated with acetyl-CoA syn- regulatory system CorQR. Similar to CooA, RcoM, whose thase (ACS); and CODH-IV, oxidative stress response (Wu gene is adjacent to CODH and ECH gene clusters in the et al. 2005; Svetlitchnyi et al. 2001). CODH-V does not con- hydrogenogenic carboxydotroph Rubrivivax gelatinosus serve sequences responsible for its active center, and hence, (phylum Proteobacteria) (Wawrousek et al. 2014), possesses its physiological function remains unknown (Inoue et al. a potential CO-sensor domain-containing heme (Kerby et al. 2013). cooS-I is arranged in a gene cluster with genes coding 2008). CorQR pair is composed of CorQ with a DNA-bind- for an electron transfer protein (CooF) (Kerby et al. 1992), ing domain of LysR-type transcriptional regulator (LTTR) Ni insertion protein (CooC) (Kerby et al. 1997), a transcrip- family and CorR with 4-vinyl reductase domain instead tional factor (CooA) (Shelver et al. 1995), and ECH-related of heme to sense CO (Kim et al. 2015). Genes encoding genes. In most hydrogenogenic carboxydotrophs, cooS-I and CorQR pair also fanked with CODH−ECH gene cluster in ECH-related genes form a gene cluster (CODH−ECH gene the hydrogenogenic carboxydotrophic archaeon, Thermococ- cluster) or are closely arranged (Sokolova et al. 2009). The cus onnurineus (phylum Euryarchaeota) (Kim et al. 2015). hydrogenogenic CO utilization is performed by a complex To date, only a few transcriptional studies about hydrog- of three enzymes; CODH-I, CooF, and ECH complex. CO enogenic CO metabolism have been reported. A transcrip- is oxidized by CODH-I and the generated electron is trans- tomic analysis of the sulfate-reducing carboxydotroph ferred to CooF. Subsequently, this electron is coupled to Desulfovibrio vulgaris using microarray reports that the proton reduction via the ECH complex, producing H2 and expression of cooS is dependent on active CooA under forming a proton gradient (Svetlitchnyi et al. 2001; Soboh low CO concentration (Rajeev et al. 2012). In addition, et al. 2002). genome-wide primary transcriptomic analysis of T. onnu- Transcription of the genes in the CODH gene cluster rineus reports that the expression of cooS is signifcantly in hydrogenogenic CO metabolism is activated by CO- upregulated when they utilize CO as the source of energy for responsive transcriptional factors CooA, RcoM (Kerby et al. H2 production (Cho et al. 2017). However, there are limited 2008), and CorQR (Kim et al. 2015). Of these, CooA is well data on comprehensive gene expression pattern of hydrog- characterized in the hydrogenogenic carboxydotroph, Rho- enogenic CO
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